InEvolution: A Theory in Crisis (Evolution), published in 1985, I argued that the biological realm is fundamentally discontinuous.1 The major taxa-defining innovations in the history of life have not been derived from ancestral forms by functional intermediates. This is the view that Sir D’Arcy Wentworth Thompson defended in On Growth and Form:

In short nature proceeds “from one type to another” [emphasis added] among organic as well as inorganic forms; and these types vary according to their own parameters, and are defined by physical-mathematical conditions of possibility. In natural history Cuvier’s “types” may not be perfectly chosen nor numerous enough but “types” they are; and to seek for stepping stones across the gaps between is to seek in vain, for ever.2

The contrary view remained predominant among evolutionary biologists until, at least, the 1980s, and remains predominant as the view offered the public today.

There have been massive advances and discoveries in many areas of biology since Evolution was first published. These developments have transformed biology and evolutionary thought. Yet orthodox evolutionary theory is unable to explain the origins of various taxa-defining innovations.

This was my position in Evolution.

It remains my position today

The Galápagos Islands

Six hundred miles off the west coast of South America lies a small archipelago consisting of nineteen barren volcanic islands scattered over a circle of sea, some one hundred and fifty miles across. The largest is about the size of Rhode Island, and four others are about one fourth this size, but most are far smaller, and some are mere rocky outcrops. Volcanic craters reaching up to three or four thousand feet surmount many of the larger islands. Because of the Humboldt Current, the climate is remarkably cool for islands straddling the Equator. The Humboldt also brings rich nutrients to the surrounding seas, which teem with marine life. Little rain falls on the arid coastal strips. Well-vegetated areas are restricted to the central higher regions, often bathed in damp clouds. The islands are fringed in places by steep cliffs, in other places by flat rocky lava flows. Occasional sandy bays provide access from the sea.

Of all the unique species of the archipelago, none were more critical to the development of Darwin’s views than the now-celebrated finches. The thirteen unique species are obviously related to one another. They exhibit the same nest architecture, egg coloration, and complex courtship display. Each species is adapted to a particular ecological niche on one or several of the islands. “Seeing this gradation and diversity of structure in one small, intimately related group of birds,” Darwin remarked, “one might really fancy that from an original paucity of birds in this archipelago, one species had been taken and modified for different ends.”3 In this conjecture, he was correct. Existing species had descended with modification from earlier species. DNA studies confirm that these species are, indeed, closely related.4

Moreover, the developmental processes and genes involved in generating the differences in beak morphology in the different species of finches are currently subject to intensive study. And the evidence to date suggests that only a relatively small number of genes, organized into two independent gene expression modules (developmental pathways), are involved in generating most of the differences in the morphology of the beaks of the finches (and other bird species). From the emerging developmental genetic picture, it is now relatively easy to envisage how gradual adaptive fine-tuning of the expression patterns of a handful of genes could result in the different beak forms of the Galápagos finches we see today.5

The evolution of finch beaks requires no causal agency beyond natural selection. Some finch beaks proved advantageous; others, not. The lesson of the Galápagos, and all such cases of microevolution, is that cumulative selection will work its magic just so long as there is an empirically known or plausible functional continuum, at the morphological or genetic level, leading from an ancestral species or structure to a descendent species or structure.

If Darwin had gone no further than providing an explanation for the evolution of the finch, he might today be remembered as a notable Victorian naturalist. But Darwin went much further. The origin and evolution of all the novelties in the history of life, he held, could be explained by extending, over long periods of time, the same simple mechanism of cumulative selection that fashioned the different species of finches on the Galápagos.

The Hierarchy of Nature

The discovery that the living world is organized into a hierarchy of ever more inclusive classes or types, each very clearly defined by a unique suite of properties, was one of the major achievements of pre-Darwinian biology. Virtually all pre-Darwinian biologists, and many after Darwin, too, saw these types as immanent parts of the world order, comparable in their way to crystals or atoms. The widespread impression that pre-Darwinian biologists derived their conclusions from discredited metaphysical assumptions is a myth. Their concept of the taxa as basic natural forms, as Ronald Amundson noted, was based on solid empirical observations. “We will fret over their metaphysics,” he remarked, “no more than we fret over Kepler’s.”6

Terrestrial vertebrates and their aquatic descendants such as whales, seals, or ichthyosaurs, possess a unique defining homology known as the pentadactyl limb, consisting of a proximal bone, two more distal bones, and five digits. These organisms are grouped together in the Tetrapoda. Modern birds, and some related groups of reptiles, possess closed pennaceous contour feathers consisting of a central shaft, or rachis. Fused to the rachis are barbs, and attached to each barb are hooked distal barbules pointing toward the tip of the feather and interlocking grooved proximal barbs pointing to the base.7 All extant organisms possessing this defining feature can be unambiguously assigned to the Aves.

Living insects also possess a set of unique defining features. Their bodies are uniformly divided into a head, a thorax, and an abdomen. The thorax consists of three segments, and each bears a pair of legs, making six altogether. Eleven segments can be recognized in the abdomen of most juvenile insects, and although some insect adults (including beetles, wasps, bees, and ants) have less than eleven, no insect has more. The legs of all insects consist of five components: the coxa, the trochanter, the femur, the tibia, and the tarsus. The tarsus itself is typically divided into five subsegments. The insect mouth always comprises four parts from front to back: the labrum, the mandibles, the maxillae, and the labium. And all insects possess two antennae. Invertebrates that possess these defining features can be unambiguously assigned to the Insecta, and all wings in extant insect species are based on the same underlying venation pattern.

The defining novelty of all angiosperms is the flower, consisting of a remarkable pattern of four nested concentric whorls: an outermost whorl of sepals surrounding a whorl of petals, which in turn surrounds a ring of stamens and, in the center, a small circular region containing the pistil. Moreover, each angiosperm subgroup is defined by a novel floral formula, a variation on the basic flower theme, indicating the defining number and variation in sepal, petal, stamen, and carpel pattern characteristic of that subgroup.

The amniotic egg, possessed by all members of the Amniota, comprising reptiles, birds, and mammals, is a defining feature of this taxon and has no antecedent structure in any ancestral form. In the case of the Mammalia, some of the defining traits are hair, an enucleate red cell, a diaphragm, mammary glands, and a laminar cerebral cortex consisting of six layers. No other vertebrate group possesses these defining features.

It is not just the major taxa that are characterized by unique defining homologs or novelties. Centipedes belonging to the Chilopoda possess two remarkable novelties. Segment number in centipede species varies from twenty-seven to one hundred and ninety-one, but in every case the segment number is odd. No centipede with an even number of segments has ever been found. And every centipede possesses a novel venom-injecting device, a poison claw. “No animals outside the Chilopoda,” Arthur Wallace observed, “possess a similar poison claw segment.” This innovation, he added, “appears to have arisen only once in evolution and, at least as yet, has persisted in all the lineages that have descended from the original ‘ur-centipede.’”8

Like all insects, every beetle has three thoracic segments, but these exhibit a unique morphology. The first segment, the prothorax, is distinct from and articulates freely with the second, the mesothorax, which is fused with the third, the metathorax, to form the pterothorax, which is in turn broadly fused to the abdomen. In the case of beetles, the coxa, the proximal segment of the leg, is recessed into a cavity formed by heavily sclerotized thoracic sclerites. The antennae nearly always consist of eleven or fewer segments, and the terminal genitalic appendages are retracted into the abdomen and invisible at rest.

The Life Cycle of the European Eel

Individual species, as well as taxa, are often defined by unique and bizarre evolutionary innovations. Sigmund Freud is best known as the founding father of psychoanalysis, but curiously, his first scientific paper dealt with the reproductive biology of the European eel. No one had seen eels mate or spawn; the breeding grounds where this took place were unknown; the early stages of development had never been observed. Adding to the mystery, no male eel had been definitively identified. Working at a marine laboratory in Trieste during the summer of 1876, Freud dissected many hundreds of eels in an attempt to identify the male gonad and to throw some light on its mysterious reproduction and life cycle. Freud failed to identify the male organs in any of the eels he dissected that summer, and after three months, he abandoned the research in frustration to seek a career in another branch of science.

It is not surprising that Freud failed to identify male sex organs in the European eel. We now know that sex determination in mature eels is a manifestly baroque phenomenon, one of the most far-fetched in any vertebrate, and determined by environmental factors that are still not fully understood.9 Extraordinary as it may seem, in some places the number of males vastly outnumbers the number of females, but in other places it is the reverse. In some studies, eels furthest from the sea tend to be females, and those nearest the sea, males.10 Both sexes pass through successive phases of neutrality and juvenile hermaphroditism before finally becoming definitely male or female.11

Their life cycle is no less elaborate than their sexual development. Although the juvenile stages had been familiar to fishermen for centuries as small, transparent, ribbon-shaped fish, until researchers first observed their transformation into recognizable eels in aquariums in the 1890s, these larval forms were considered entirely different species. Heroic efforts by the Danish researcher Johannes Schmidt, between 1905 and 1930, showed that the very smallest eels were found in the region of the Atlantic known as the Sargasso Sea. This warm body of water off the east coast of the United States was eventually accepted as their spawning grounds.12

Although no one has observed the mating and spawning of European eels in the wild, their life cycle is now understood in outline. After the eggs hatch in the Sargasso Sea, the tiny larvae travel four thousand miles to the shores of Europe, over a period of two and a half years. As they near the coast, they lose their sharp juvenile teeth and stop feeding; the anus migrates from a subterminal position to the abdominal midpoint, and they lose skin pigment, metamorphosing into the well-known cylindrical glass eels, or juvenile elvers, that collect in vast numbers in the estuaries and river mouths of western Europe.13 In the autumn, the elvers begin their familiar migration in countless numbers up the European rivers, gradually losing their glass-like appearance as color starts to reappear in their skin and they take on the more familiar appearance of young eels. During this migration, they may travel across wet grass and even dig through wet sand to satisfy their urge to reach upstream headwaters and ponds, thus eventually colonizing every river and small body of water in western Europe.

Over the next ten years, they grow to a length of up to eighty centimeters in females, forty centimeters in males, and develop a golden pigmentation, hence “yellow eels.” Males remain in the rivers for about six years before returning to the sea, while females remain for about nine years. Mature European eels begin their migration back to the Sargasso Sea in July. On leaving for their return journey, their gut degenerates. They stop feeding. Their eyes enlarge; their eye pigments change for optimal vision in dim, blue, clear, ocean light. Their skin lightens on their sides and ventral surface and darkens on their back to create a countershading pattern, making it difficult for predators to see them during their long open ocean migration.14 How they manage the journey back to the Sargasso Sea without feeding and against the current is unknown. To date, no adult eel has ever been followed from the European shores back to the Sargasso Sea.

The evolutionary factors responsible for such an extraordinarily roundabout way of reproducing are mystifying. What tiny adaptive steps led from the reproductive habits of a normal fish to such a grotesque life cycle? What adaptive significance do such sexual metamorphoses serve? What selective pressures led the adult eels to dissolve their guts and stop feeding to make the journey back to the Sargasso Sea? Why does the anus migrate from the tail to mid-abdomen during the final stages of larval maturation? Why do males stay in Europe for six years and females for nine before returning to the ocean? What selective advantage did eels achieve by making the transition from salt to fresh water? What conceivable “long series of gradations ... each good for its possessor” could possibly have orchestrated the whole performance?15 I think it would be hard to invent a story more difficult to comprehend in terms of cumulative selection.

The existence of genuine novelties in living systems is very widely conceded; it is also widely acknowledged that explaining how novelties arise is one of the key problems that evolutionary biology must address.

In Evolution, I argued that:

The same deep homologous resemblance which serves to link all the members of one class together into a natural group also serves to distinguish that class unambiguously from all other classes. Similarly, the same hierarchic pattern, which may be explained in terms of a theory of common descent, also, by its very nature, implies the existence of deep divisions in the order of nature. The same facts of comparative anatomy which proclaim unity also proclaim division; while resemblance suggests evolution, division, especially where it appears profound, is counter-evidence against the whole notion of gradual transmutation.16

Today, thirty years later, despite the discovery of a huge number of new fossil forms, it is still true, as Darwin confessed, that “the distinctness of specific forms ... not ... blended together by innumerable transitional links is a very obvious difficulty.”17

Non-Adaptive Order

Evolutionary novelties pose one obvious challenge to Darwinian theories. The fact that, in most cases, their adaptive status is clearly in doubt poses another. This is the argument of Richard Owen’s On the Nature of Limbs. Owen opens his great work by alluding to the very different types of adaptive masks—the term is his—that vertebrates have worn in locomotion: the fin of the dugong, the forelimb of the mole, the wing of a bat, and the limb of a horse. He shows, by illustrations of their individual skeletal designs, that they are all based on a single original design: what he termed a “primal pattern.”

What is very surprising is that the pentadactyl limb, or underlying primal pattern, gives no clear indication of having ever served an adaptive purpose. The situation is strikingly different when human and organic technologies are compared:

To break his ocean-bounds the islander fabricates his craft, and glides over the water by means of the oar, the sail, or the paddle-wheel. To quit the dull earth Man inflates the balloon, and soars aloft, and perhaps, endeavors to steer or guide his course by the action of broad expanded sheets, like wings. With the arched shield, and the spade or pick, he bores the tunnel: and his modes of accelerating his speed in moving over the surface of the ground are many and various. But whatever means or instruments Man aids, or supersedes, his natural locomotive organs, such instruments are adapted expressly and immediately to the end proposed. He does not fetter himself by the trammels of any common type of locomotive instrument, and increase his pains by having to adjust the parts and compensate their proportions, so as best to perform the end required without deviating from the pattern previously laid down for all. There is no community of plan or structure between the boat and the balloon, between Stephenson’s engine and Brunei’s tunneling machinery: a very remote analogy, if any, can be traced between the instruments devised by man to travel in the air and on the sea, through the earth or along its surface.18

Owen then makes a decisive point:

Nor should we anticipate, if animated in our researchers by the quest of final causes in the belief that they were the sole governing principle of organization, a much greater amount of conformity in the construction of the natural instruments by means of which those different elements are traversed by different animals. The teleologist would rather expect to find the same direct and purposive adaptation of the limb to its office as in the machine. A deep and pregnant principle in philosophy, therefore, is concerned in the issue of such dissections, and to these, therefore I now pass, premising that the end in view will be attained without extending the comparison beyond the framework of the limbs, or the leverage of the bones and joints.19

If it is the various adaptive masks adopted for swimming, flying, grasping, and running that serve adaptive ends, then it becomes very difficult to grasp the adaptive purpose of the underlying primal pattern itself. Neither Owen nor any of the other pre-Darwinian biologists denied the fact of adaptation or its significance, but they saw in adaptation a secondary phenomenon, the response to environmental conditions.

Adaptation, they concluded, is not the only or even the primary organizational principle in biology.

Abstract Patterns

A great many of the taxa-defining novelties in living systems convey the impression of being entirely abstract. Curious geometric and numerical patterns permeate the biological realm. Nearly all mammals have seven cervical vertebrae, and all have six distinct layers of cells in their cerebral cortex. As noted above, all insects are divided into three main body segments. Their legs have five divisions. All longicorn beetles have eleven joints in their antennae, except for the longicorn Prionidae, most of which have the unusual number of twelve antennary joints.20 Nearly all fruit flies have twenty pairs of bristles on their backs, all placed in precisely the same geometric position in every individual.21

Consider wing venation patterns in the Nymphalid butterflies. An early text offers a terse, telegraphic impression:

The forewing: the submedial, or vein 1, simple, [unbranched] in one subfamily forked near base; medial vein with three branches, veins 2, 3 and 4; veins 5 and 6 arising from the points of junction of the discocellulars; subcostal vein and its continuation beyond apex of cell, vein 7, with never more than four branches, veins 8–11; 8 and 9 always arising from vein 7, 10 and also 11 sometimes from vein 7 but more often free, i.e. given off by the subcostal vein before apex of cell.22

The texts of invertebrate paleontology contain similar observations. Principles of Invertebrate Paleontology, by Robert Shrock and William Twenhofel, one of the classic texts in the field, has examples on nearly every page.23 The number of segments making up the various parts of the body of different groups of fossil arthropods, including shrimps, lobsters, trilobites, and spiders, is fantastically variable, yet each group almost always has the same number of segments in each body part despite the bizarre and complex variation in its lifestyle and adaptations. On even a cursory consideration of the vast inventory of invertebrate type-defining novelties described in this major work, it would appear that the great majority serve no adaptive purpose.

The difficulty of accounting for such arbitrary geometric and numerical patterns in terms of bit-by-bit selection was one of the arguments used by William Bateson in a devastating critique of Darwinism in his Materials for the Study of Variation. He asks whether it “would be expected that the Longicorn Prionidae, most of which have the unusual number of 12 antennary joints, did, as they separated from other Longicorns, which have 11 joints, gradually first acquire a new joint as a rudiment, which in successive generations increased?”24 There are, Bateson observed, “hundreds of like examples in arthropods.”25 What Bateson called “Continuity in Variation” leads, he suggested, “into endless absurdity.”26

If a significant proportion of the taxa-defining patterns serve no specific function, as Owen argued in the case of the tetrapod limb, then cumulative selection cannot provide an explanation for the origin of a significant fraction of the defining homologs, and hence for the natural system itself.

The existence of a vast universe of non-adaptive forms raises one problem, and it suggests another. On what grounds can the homologous patterns, such as the pentadactyl limb or the concentric whorls of the angiosperm flower, be distinguished from patterns that no one doubts are abstract? “The forces that bring about the sphere, the cylinder or the ellipsoid,” Thompson remarked uncontroversially, “are the same yesterday and tomorrow. A snow-crystal is the same to-day as when the first snows fell.” By the same token, “the physical forces which mold the forms of Orbulina, of Astrorhiza, of Lagena or of Nodosaria to-day were still the same, and for aught we have reason to believe the physical conditions under which they worked were not appreciably different, in that yesterday we call the Cretaceous.”27

Stephen Jay Gould draws the obvious conclusion that “[t]hese forms are ... no more ... subject to specific accounts of historical filiation, than are the varied shapes of snowflakes or quartz crystals.”28

Evolutionary Developmental Biology

One of the major advances since the publication of Evolution has been the increase in our understanding of developmental genetics. It would appear that a limited set of genes and developmental mechanisms, what Sean Carroll referred to in his book Endless Forms Most Beautiful as “the universal toolkit,” are involved in the generation of all the types, body plans, and deep homologies actualized over the course of evolutionary history.29 For example, in all animal groups, the Pax6 gene turns on the genetic machinery that leads to the development of the eye, even though the eyes of insects and vertebrates could hardly be more different in design. Equally remarkable is the fact that a set of closely related genes, the Hox genes, determines segment identity in all animal species. Moreover, they are arranged in a linear sequence in the DNA of all known higher animals. And amazingly, their expression and function along the anterior-posterior body axis are the same as their order in the DNA. “The conservation of a set of clustered genes over half a billion years,” Rudolf Raff observed, “is difficult enough to accept, but colinearity with body axis defies credibility.”30

A remarkable experiment, described in Neil Shubin’s Your Inner Fish, demonstrated how one conserved toolkit component, a signaling molecule known as “sonic hedgehog protein,” had the same effect on the development of shark fins as on mammalian and chicken digits. Shubin was suitably impressed by this remarkable result. “It means,” he observed, “that this great evolutionary transformation [from fish fins into limbs] did not involve the origin of new DNA.”31 Old wine had, instead, been poured into new bottles. “Much of the shift likely involved using ancient genes, such as those involved in shark fin development, in new ways to make limbs with fingers and toes.”32 This view is today widespread among researchers in evolutionary developmental biology, known as evo-devo.

One of the most widely utilized tools of biology’s universal toolkit is diffusion-driven instability, first proposed by Alan Turing, known better as a code-breaker and mathematical logician than as a theoretical biologist. He showed that if certain quite specific constraints are satisfied, two chemicals, reacting and diffusing on some domain, may form spatially heterogeneous patterns of chemical concentration. Turing’s reaction–diffusion model has been found to be involved in generating many biological patterns, including fish pigmentation and the spatial arrangement of feather buds, reptile scales, and hair follicles.

A specific example is the co-option of an ancient, deeply conserved Turing reaction–diffusion mechanism involved in fin morphogenesis to generate the fingers in the tetrapod limb. As Rushikesh Sheth et al. remark in a recent study of mouse digit development:

The periodic pattern of skeletal elements evident in fins and mutant limbs strongly suggests that a self-organizing Turing-type mechanism of chondrogenesis is deeply conserved in vertebrate phylogeny. Our results further indicate that distal Hox gene dose regulates the number and spacing of skeletal elements formed, implicating distal Hox gene regulatory networks as critical drivers of the evolution of the pentadactyl limb ... Thus, our data provide evidence that an ancestral Turing-like mechanism patterning fins has been conserved in tetrapods and modified by the implementation of regulatory changes in the evolution of digits.33

The discovery of very widely conserved genes and developmental pathways provides powerful support for the concept of descent with modification. But descent with modification has never been in doubt since Alfred Russel Wallace’s famous “Sarawak Law” paper, which was written in Borneo in February 1855. “Every species,” Wallace observed, “has come into existence coincident both in space and time with a pre-existing closely allied species.”

The fact that the same toolkit is used universally supports descent with modification, but it does not explain how relevant novelties came about during decent with modification, or whether they were adaptive. That sugar and carbonic acid are composed of the same atoms does not imply that sugar can be converted into carbonic acid by means of a series of individual atomic steps; and that the same atoms, proteins, cell types, gene circuits, gradients, and Turing mechanisms are used to make fins, hands, reptile scales, feathers, fir cones, and flowers does not imply anything beyond the obvious fact that these structures were made using a common toolkit.

Trying to envisage the actualization of these complex patterns via a long series of adaptive intermediates leads again to Bateson’s “endless absurdity.”

The Enucleate Red Cell

One of the simplest of all the defining homologs of any major taxon is the mammalian enucleate red blood cell. Shared by monotremes, marsupials, and placentals, it must have been an ancient novelty originating in the common ancestor of all mammalian species.

The final differentiation of the red cell within an organism involves two very different types of change. A series of incremental changes leads from the large nucleated erythroid stem cell through several cell divisions to the normoblast. The nucleus of the normoblast is then ejected from the normoblast itself, a spectacular saltation resulting in the classic and iconic enucleate red blood cell.

But this is simply the big picture. The process itself is extremely complex, as any number of specialists, such as Narla Mohandas, have observed:

Enucleation is a multistep process ... that requires displacement of the nucleus in the erythroblast to one side during the preparatory stage. This is followed by formation of a contractile actin ring, pinching off the nascent reticulocyte from the nucleus, and subsequent redistribution of membrane between the 2 lobes of the dividing cell by vesicle shuttling to restrict the area of contact between the 2 emerging cells. The coordinated execution of these diverse events during a period of 8 to 10 minutes requires complex machinery embracing a number of distinct cytoskeletal proteins and signaling interventions.34

Virtually all of the cell’s basic cytological machinery is co-opted in absolutely unique ways to push the nucleus to the periphery of the cell and eventually out of the cell. As Ganesan Keerthivasan et al. explain in a recent paper, the process involves the formation of an actin cytoskeleton that pushes the nucleus to one pole; vesicular trafficking creating asymmetric protein distribution in the cytoplasm; protrusion of the plasma membrane surrounding the condensed nucleus along with the nucleus; accumulation of vesicles and vacuoles in the region between nucleus and cytoplasm; and their coalescence into U-shaped channels, which facilitates the separation of the reticulocyte from the nucleus.35 And as they comment, the process is only superficially similar to ordinary cytokinesis or cell division: “Even though the final stages of cytokinesis and enucleation are both driven by vesicle trafficking, the preceding events are substantially different between the two processes. [emphasis added]” 36

This is not all. Extruding the nucleus involves complex changes to the membrane structure in the region where the nucleus is sited immediately before enucleation. “The membrane that is destined to enclose [the] pyrenocyte [the extruded nucleus] that is in close proximity to nucleus lacks actin cytoskeleton, spectrin, and other critical proteins and as a result can be visualized to balloon out without resisting the pressure exerted by the cytoskeletal activity.”37 Furthermore, the plasma membrane that comes to surround the nucleus immediately before extrusion becomes coated with phosphatidyl serine on its surface, “ ...providing an ‘eat me’ signal for macrophages, which engulf them.”38

There is still much to learn about the cellular mechanisms involved in red cell enucleation. Despite years of intense study, as Junxia Wang et al. concede in another recent paper, many of the molecular events involved remain unclear.39

The enucleation of the red cell illustrates nicely the co-option of existing cellular elements for novel ends. As we have seen above, this is one of the themes of evo-devo, highlighted in Carroll’s Endless Forms Most Beautiful. It is certainly true that the machinery of enucleation makes use of existing cytological elements, mechanisms, and processes. A grab bag would include actin and myosin molecules, vesicles and vesicle transport, microtubules, intermediate fibers, spectrin and other membrane proteins, the formation of a contractile rim, the formation of a multivesicular gap between the nucleus and main remaining body of the cytoplasm, the change in the cell membrane structure around the nucleus, the connecting bleb full of actin fibers pushing the nucleus out of the cell, and so forth. But the unique way in which these items are co-opted toward enucleation illustrates just how empty such a claim is, providing, as it does, no explanation for the novelty itself.

There is no known intermediate type of cell midway between the enucleate cell and the nucleated red cells of any other vertebrate species. As I argued in Evolution, where there is an empirical absence of transitional forms, envisaging plausible hypothetical intermediates invariably proves impossible. And so it is here.

Vertebrate erythrocytes are either nucleated or enucleated. But without intermediates or partially enucleated cells, there would be no way of approaching the enucleate state gradually. If there are no intermediates, then the utility of the enucleate red cell could only have been tested when the enucleate cell enters the bloodstream and is forced through the smallest capillaries. The very first test of the utility of the enucleate red cell could only have been carried out after the complex and unique machinery for pushing out the nucleus was already in place.

Moreover, I have been assuming for the sake of argument that the final enucleate cell is adaptive because it is better able to navigate the very narrow capillaries, and hence deliver oxygen to the tissues more efficiently. “To fulfill the requirements of shape and flexibility,” Mohandas has argued, “combined with mechanical stability, the nucleated precursor must dispose of its nucleus.”40 This is the canonical explanation for enucleation.

Mohandas and other authors may well be right, but a number of considerations undermine this account. In the early stages of mammalian embryogenesis, where the demand for oxygen is high and when the major species of hemoglobin have a higher affinity for oxygen than in adult mammals, nucleated red cells do enter the circulation. Furthermore, birds, which have a higher metabolic need for oxygen than mammals, retain their nucleus. Anyone who has watched a hummingbird sucking nectar from a flower or geese flying over the Himalayas will have been struck by the incredible ability of birds to deliver oxygen to their muscles to empower flight, even at conditions of greatly reduced oxygen partial pressure. If birds get by with nucleated cells, perhaps the enucleate state is not as specifically adaptive as widely imagined. There are further considerations suggesting this novelty, one of the defining characteristics of the Mammalia, is beyond any simple adaptive explanation. The size of the various red blood cells in different species of mammals varies in ways that have never been explained in adaptive terms. In the case of the mouse deer, the red cell is two microns across, less than a third of the diameter of a human red cell.41 Why have our cells remained so huge and relatively immobile compared with those of a mouse deer?

The enucleate red blood cell is an anomaly, one that if it stood alone, would be nothing more than a puzzle. Every scientific theory faces such puzzles. But it does not stand alone. It is one of a series of comparable anomalies and these sum collectively to something far more than a puzzle.

Charles Darwin, Journal of Researches into the Natural History and Geology of the Countries Visited During the Voyage of H.M.S. Beagle Round the World, Under the Command of Capt. Fitz Roy, R.N. (London: John Murray, 1845), 380. &larrhk;

Akie Sato et al., “Phylogeny of Darwin’s Finches as Revealed by mtDNA Sequences,” Proceedings of the National Academy of Sciences of the United States of America 96, no. 9 (1999): 5101–06.&larrhk;

Ricardo Mallarino et al., “Two Developmental Modules Establish 3D Beak-Shape Variation in Darwin’s Finches,” Proceedings of the National Academy of Sciences of the United States of America 108, no. 10 (2011): 4057–62. &larrhk;

Ronald Amundson, The Changing Role of the Embryo in Evolutionary Thought: Roots of Evo-Devo (Cambridge: Cambridge University Press, 2005), 18. &larrhk;